Compound-specific stable isotope analyses of fatty acids indicate feeding zones of zooplankton across the water column of a subalpine lake

. 2024 Jun ; 205 (2) : 325-337. [epub] 20240603

Jazyk angličtina Země Německo Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38829405

Grantová podpora
Lake Lunz long-term ecological research grant Amt der NÖ Landesregierung

Odkazy

PubMed 38829405
PubMed Central PMC11628586
DOI 10.1007/s00442-024-05574-3
PII: 10.1007/s00442-024-05574-3
Knihovny.cz E-zdroje

Spatial and temporal zooplankton feeding dynamics across the water column of lakes are key for understanding site-specific acquisition of diet sources. During this 6-week lake study, we examined stable carbon (δ13C) and nitrogen (δ15N) isotopes and conducted compound-specific fatty acid (FA) stable isotope analysis (CSIA) of edible seston in the epi-, meta-, and hypolimnion, and zooplankton of Lake Lunz, Austria. We predicted that CSIA of essential FA can discern the foraging grounds of zooplankton more accurately than the commonly used bulk stable isotopes. The δ13C and δ15N values of seston from different lake strata were similar, whereas a dual CSIA approach using stable carbon and hydrogen isotopes of FA (δ13CFA and δ2HFA) provided sufficient isotopic difference in essential FA to discern different lake strata-specific diet sources throughout the study period. We present a CSIA model that suggests strata-specific foraging grounds for different zooplankton groups, indicating higher preference of cladocerans for feeding on epilimnetic diet sources, while calanoid copepods retained more hypolimnetic resources. The CSIA approach thus yields strata-specific information on foraging strategies of different zooplankton taxa and provides more details on the spatial and temporal trophodynamics of planktonic food webs than commonly used bulk stable isotopes.

Zobrazit více v PubMed

Adrian R (1997) Calanoid–cyclopoid interactions: evidence from an 11-year field study in a eutrophic lake. Freshw Biol 38:315–325. 10.1046/j.1365-2427.1997.00215.x

Balseiro EG, Modenutti BE, Queimaliños CP (2001) Feeding of Boeckella gracilipes (Copepoda, Calanoida) on ciliates and phytoflagellates in an ultraoligotrophic Andean lake. J Plankton Res 23:849–857. 10.1093/plankt/23.8.849

Burian A, Nielsen JM, Hansen T, Bermudez R, Winder M (2020) The potential of fatty acid isotopes to trace trophic transfer in aquatic food-webs. Philos Trans R Soc B Biol Sci. 10.1098/rstb.2019.0652 PubMed PMC

Burns CW (1968) The relationship between body size of filter-feeding cladocera and the maximum size of particle ingested. Limnol Oceanogr 13:675–678. 10.4319/lo.1968.13.4.0675

Burns C, Brett M, Schallenberg M (2010) A comparison of the trophic transfer of fatty acids in freshwater plankton by cladocerans and calanoid copepods. Freshw Biol 56:889–903. 10.1111/j.1365-2427.2010.02534.x

Calderó-Pascual M, de Eyto E, Jennings E, Dillane M, Andersen MR, Kelly S, Wilson HL, McCarthy V (2020) Effects of consecutive extreme weather events on a temperate dystrophic lake: a detailed insight into physical. Chem Biol Responses Water 12:1411. 10.3390/w12051411

Castro LFC, Tocher DR, Monroig O (2016) Long-chain polyunsaturated fatty acid biosynthesis in chordates: insights into the evolution of Fads and Elovl gene repertoire. Prog Lipid Res 62:25–40. 10.1016/j.plipres.2016.01.001 PubMed

Copeman LA, Parrish CC, Brown JA, Harel M (2002) Effects of docosahexaenoic, eicosapentaenoic, and arachidonic acids on the early growth, survival, lipid composition and pigmentation of yellowtail flounder (Limanda ferruginea): a live food enrichment experiment. Aquaculture 210:285–304. 10.1016/S0044-8486(01)00849-3

De Troch M, Boeckx P, Cnudde C, Gansbeke D, Vanreusel A, Vincx M, Caramujo M (2012) Bioconversion of fatty acids at the basis of marine food webs: insights from a compound-specific stable isotope analysis. Mar Ecol Prog Ser 465:53–67. 10.3354/meps09920

Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251. 10.1126/science.1061967 PubMed

Gladyshev MI, Semenchenko VP, Dubovskaya OP, Fefilova EB, Makhutova ON, Buseva ZF, Sushchik NN, Razlutskij VI, Lepskaya EV, Baturina MA, Kalachova GS, Kononova ON (2011) Effect of temperature on contents of essential highly unsaturated fatty acids in freshwater zooplankton. Limnologica 41:339–347. 10.1016/j.limno.2011.03.001 PubMed

Harvey CJ, Kitchell JF (2000) A stable isotope evaluation of the structure and spatial heterogeneity of a lake superior food web. Can J Fish Aquat Sci 57:1395–1403. 10.1139/f00-072

Ikeda T (1985) Metabolic rates of epipelagic marine zooplankton as a function of body mass and temperature. Mar Biol 85:1–11. 10.1007/BF00396409

Kainz MJ, Hager HH, Rasconi S, Kahilainen KK, Amundsen P-A, Hayden B (2017) Polyunsaturated fatty acids in fishes increase with total lipids irrespective of feeding sources and trophic position. Ecosphere 8:e01753. 10.1002/ecs2.1753

Kasprzak P, Reese C, Koschel R, Schulz M, Hambaryan L, Mathes J (2005) Habitat characteristics of Eurytemora lacustris (Poppe, 1887) (Copepoda, Calanoida): the role of lake depth, temperature, oxygen concentration and light intensity. Int Rev Hydrobiol 90:292–309. 10.1002/iroh.200410769

Kasprzak P, Shatwell T, Gessner MO, Gonsiorczyk T, Kirillin G, Selmeczy G, Padisák J, Engelhardt C (2017) Extreme weather event triggers cascade towards extreme turbidity in a clear-water lake. Ecosystems 20:1407–1420. 10.1007/s10021-017-0121-4

Koenings JP, Burkett RD, Edmundson JM (1990) The exclusion of limnetic cladocera from turbid glacier-meltwater lakes. Ecology 71:57–67. 10.2307/1940247

Kohlbach D, Lebreton B, Guillou G, Wold A, Hop H, Graeve M, Assmy P (2023) Dependency of arctic zooplankton on pelagic food sources: new insights from fatty acid and stable isotope analyses. Limnol Oceanogr 68:2346–2358. 10.1002/lno.12423

Koussoroplis A-M, Kainz MJ, Striebel M (2013) Fatty acid retention under temporally heterogeneous dietary intake in a cladoceran. Oikos 122:1017–1026. 10.1111/j.1600-0706.2012.20759.x

Koussoroplis A-M, Nussbaumer J, Arts MT, Guschina IA, Kainz MJ (2014) Famine and feast in a common freshwater calanoid: Effects of diet and temperature on fatty acid dynamics of Eudiaptomus gracilis. Limnol Oceanogr 59:947–958. 10.4319/lo.2014.59.3.0947

Kürten B, Frutos I, Struck U, Painting SJ, Polunin NVC, Middelburg JJ (2013) Trophodynamics and functional feeding groups of north sea fauna: a combined stable isotope and fatty acid approach. Biogeochemistry 113:189–212. 10.1007/s10533-012-9701-8

Lang I, Hodac L, Friedl T, Feussner I (2011) Fatty acid profiles and their distribution patterns in microalgae: a comprehensive analysis of more than 2000 strains from the SAG culture collection. BMC Plant Biol 11:124. 10.1186/1471-2229-11-124 PubMed PMC

Lee J-Y, Kim J-K, Owen JS, Choi Y, Shin K, Jung S, Kim B (2013) Variation in carbon and nitrogen stable isotopes in POM and zooplankton in a deep reservoir and relationship to hydrological characteristics. J Freshw Ecol 28:47–62. 10.1080/02705060.2012.689999

Maier G (1990) Coexistence of the predatory cyclopoids Acanthocyclops robustus (Sars) and Mesocyclops leuckarti (Claus) in a small eutrophic lake. Hydrobiologia 198:185–203. 10.1007/BF00048634

Maier G (1996) Copepod communities in lakes of varying trophic degree. Arch Hydrobiol 136(4):455–465. 10.1127/archiv-hydrobiol/136/1996/455

Mathieu F, Guo F, Kainz MJ (2022) Tracking dietary fatty acids in triacylglycerols and phospholipids of zooplankton. Freshw Biol 67:1949–1959. 10.1111/fwb.13988

McCullough GK, Page SJ, Hesslein RH, Stainton MP, Kling HJ, Salki AG, Barber DG (2012) Hydrological forcing of a recent trophic surge in lake winnipeg. J Gt Lakes Res 38:95–105. 10.1016/j.jglr.2011.12.012

McMeans BC, Koussoroplis A-M, Kainz MJ (2015) Effects of seasonal seston and temperature changes on lake zooplankton fatty acids. Limnol Oceanogr 60:573–583. 10.1002/lno.10041

Morlock MA, Schilder J, van Hardenbroek M, Szidat S, Wooller MJ, Heiri O (2017) Seasonality of cladoceran and bryozoan resting stage δ13C values and implications for their use as palaeolimnological indicators of lacustrine carbon cycle dynamics. J Paleolimnol 57:141–156. 10.1007/s10933-016-9936-9

Müller-Navarra DC (2008) Food web paradigms: the biochemical view on trophic interactions. Int Rev Hydrobiol 93:489–505. 10.1002/iroh.200711046

Papirńska K (1985) Carnivorous and detritivorous feeding of Mesocyclops leuckarti Claus (Cyclopoida Copepoda). Hydrobiologia 120:249–257. 10.1007/BF00045168

Parnell AC, Phillips DL, Bearhop S, Semmens BX, Ward EJ, Moore JW, Jackson AL, Grey J, Kelly DJ, Inger R (2013) Bayesian stable isotope mixing models. Environmetrics 24:387–399. 10.1002/env.2221

Pilecky M, Závorka L, Arts MT, Kainz MJ (2021) Omega-3 PUFA profoundly affect neural, physiological, and behavioural competences – implications for systemic changes in trophic interactions. Biol Rev 96:2127–2145. 10.1111/brv.12747 PubMed

Pilecky M, Fink P, Kämmer SK, Schott M, Zehl M, Kainz MJ (2022a) Mass spectrometry imaging reveals the spatial distribution of essential lipids in Daphnia magna – potential implications for trophic ecology. Inland Waters. 10.1080/20442041.2022.2127609

Pilecky M, Kämmer SK, Mathieu-Resuge M, Wassenaar LI, Taipale SJ, Martin-Creuzburg D, Kainz MJ (2022b) Hydrogen isotopes (δ2H) of polyunsaturated fatty acids track bioconversion by zooplankton. Funct Ecol 36:538–549. 10.1111/1365-2435.13981

Pilecky M, Wassenaar LI, Kainz MJ, Anparasan L, Ramirez MI, McNeil JN, Hobson KA (2022c) Isotopic (δ2H and δ13C) tracing the provenance and fate of individual fatty acids fueling migrating animals: a case study of the monarch butterfly (Danaus plexippus). Front Ecol Evol. 10.3389/fevo.2022.1051782

Pilecky M, Závorka L, Soto DX, Guo F, Wassenaar LI, Kainz MJ (2022d) Assessment of compound-specific fatty acid δ13C and δ2H values to track fish mobility in a small sub-alpine catchment. Environ Sci Technol 56:11051–11060. 10.1021/acs.est.2c02089 PubMed PMC

Pilecky M, Meador TB, Kämmer SK, Winter K, Ptacnikova R, Wassenaar LI, Kainz MJ (2023a) Response of stable isotopes (δ2H, δ13C, δ15N, δ18O) of lake water, dissolved organic matter, seston, and zooplankton to an extreme precipitation event. Sci Total Environ 891:164622. 10.1016/j.scitotenv.2023.164622 PubMed

Pilecky M, Wassenaar LI, Taipale S, Kainz MJ (2023b) Protocols for sample preparation and compound-specific stable-isotope analyses (δ2H, δ13C) of fatty acids in biological and environmental samples. MethodsX 11:102283. 10.1016/j.mex.2023.102283 PubMed PMC

Rasconi S, Ptacnik R, Kainz MJ (2018) Seston fatty acid responses to physicochemical changes in subalpine lake Lunz. Austria Water Resour Res 54:8442–8455. 10.1029/2017WR020959 PubMed PMC

Ringelberg J (1999) The photobehaviour of Daphnia spp. as a model to explain diel vertical migration in zooplankton. Biol Rev 74:397–423. 10.1111/j.1469-185X.1999.tb00036.x

Ringelberg J (2009) Diel vertical migration of zooplankton in lakes and oceans: causal explanations and adaptive significances. Springer Science & Business Media

Saage A, Vadstein O, Sommer U (2009) Feeding behaviour of adult Centropages hamatus (Copepoda, Calanoida): functional response and selective feeding experiments. J Sea Res 62:16–21. 10.1016/j.seares.2009.01.002

Santer B (1994) Influences of food type and concentration on the development of Eudiaptomus gracilis and implications for interactions between calanoid and cyclopoid copepods. Arch Für Hydrobiol. 10.1127/archiv-hydrobiol/131/1994/141

Seebens H, Einsle U, Straile D (2009) Copepod life cycle adaptations and success in response to phytoplankton spring bloom phenology. Glob Change Biol 15:1394–1404. 10.1111/j.1365-2486.2008.01806.x

Sessions AL, Burgoyne TW, Schimmelmann A, Hayes JM (1999) Fractionation of hydrogen isotopes in lipid biosynthesis. Org Geochem 30:1193–1200. 10.1016/S0146-6380(99)00094-7

Siebeck O (1960) Untersuchungen über die Vertikalwanderung Planktischer Crustaceen Unter Berücksichtigung der Strahlungsverhältnisse. Int Rev Gesamten Hydrobiol Hydrogr 45:381–454. 10.1002/iroh.19600450309

Storz UC, Paul RJ (1998) Phototaxis in water fleas (Daphnia magna) is differently influenced by visible and UV light. J Comp Physiol A 183:709–717. 10.1007/s003590050293

Taipale SJ, Kainz MJ, Brett MT (2011) Diet-switching experiments show rapid accumulation and preferential retention of highly unsaturated fatty acids in daphnia. Oikos 120:1674–1682. 10.1111/j.1600-0706.2011.19415.x

Taipale S, Strandberg U, Peltomaa E, Galloway AWE, Ojala A, Brett MT (2013) Fatty acid composition as biomarkers of freshwater microalgae: analysis of 37 strains of microalgae in 22 genera and in seven classes. Aquat Microb Ecol 71:165–178. 10.3354/ame01671

Taipale SJ, Kainz MJ, Brett MT (2015) A low ω-3:ω-6 ratio in daphnia indicates terrestrial resource utilization and poor nutritional condition. J Plankton Res 37:596–610. 10.1093/plankt/fbv015

Taipale SJ, Vuorio K, Strandberg U, Kahilainen KK, Järvinen M, Hiltunen M, Peltomaa E, Kankaala P (2016) Lake eutrophication and brownification downgrade availability and transfer of essential fatty acids for human consumption. Environ Int 96:156–166. 10.1016/j.envint.2016.08.018 PubMed

Titocci J, Fink P (2022) Food quality impacts on reproductive traits, development and fatty acid composition of the freshwater calanoid copepod Eudiaptomus sp. J Plankton Res 44:528–541. 10.1093/plankt/fbac030

Twining CW, Brenna JT, Lawrence P, Shipley JR, Tollefson TN, Winkler DW (2016) Omega-3 long-chain polyunsaturated fatty acids support aerial insectivore performance more than food quantity. Proc Natl Acad Sci 113:10920–10925. 10.1073/pnas.1603998113 PubMed PMC

Twining CW, Taipale SJ, Ruess L, Bec A, Martin-Creuzburg D, Kainz MJ (2020) Stable isotopes of fatty acids: current and future perspectives for advancing trophic ecology. Philos Trans R Soc B Biol Sci. 10.1098/rstb.2019.0641 PubMed PMC

Twining CW, Bernhardt JR, Derry AM, Hudson CM, Ishikawa A, Kabeya N, Kainz MJ, Kitano J, Kowarik C, Ladd SN, Leal MC, Scharnweber K, Shipley JR, Matthews B (2021) The evolutionary ecology of fatty-acid variation: Implications for consumer adaptation and diversification. Ecol Lett 24:1709–1731. 10.1111/ele.13771 PubMed

Vanderploeg HA, Paffenhöfer G-A (1985) Modes of algal capture by the freshwater copepod Diaptomus sicilis and their relation to food-size selection. Limnol Oceanogr 30:871–885. 10.4319/lo.1985.30.4.0871

von Elert E (2002) Determination of limiting polyunsaturated fatty acids in Daphnia galeata using a new method to enrich food algae with single fatty acids. Limnol Oceanogr 47:1764–1773. 10.4319/lo.2002.47.6.1764

Voss A, Reinhart M, Sankarappa S, Sprecher H (1991) The metabolism of 7,10,13,16,19-docosapentaenoic acid to 4,7,10,13,16,19-docosahexaenoic acid in rat liver is independent of a 4-desaturase. J Biol Chem 266:19995–20000. 10.1016/S0021-9258(18)54882-1 PubMed

Wickham SA (1995) Cyclops predation on ciliates: species-specific differences and functional responses. J Plankton Res 17:1633–1646. 10.1093/plankt/17.8.1633

Wilkinson GM, Carpenter SR, Cole JJ, Pace ML (2014) Use of deep autochthonous resources by zooplankton: Results of a metalimnetic addition of 13C to a small lake. Limnol Oceanogr 59:986–996. 10.4319/lo.2014.59.3.0986

Young JW, Hunt BPV, Cook TR, Llopiz JK, Hazen EL, Pethybridge HR, Ceccarelli D, Lorrain A, Olson RJ, Allain V, Menkes C, Patterson T, Nicol S, Lehodey P, Kloser RJ, Arrizabalaga H, Anela Choy C (2015) The trophodynamics of marine top predators: current knowledge, recent advances and challenges. Deep Sea Res Part II Top Stud 113:170–187. 10.1016/j.dsr2.2014.05.015

Zhang Z, Sachs JP (2007) Hydrogen isotope fractionation in freshwater algae: I. Variations among lipids and species. Org Geochem 38:582–608. 10.1016/j.orggeochem.2006.12.004

Zhang Z, Sachs JP, Marchetti A (2009) Hydrogen isotope fractionation in freshwater and marine algae: II. Temperature and nitrogen limited growth rate effects. Org Geochem 40:428–439. 10.1016/j.orggeochem.2008.11.002

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...